Descriptive Epidemiology of the first outbreak of Lumpy Skin Disease in cattle in Indonesia

doi:10.21203/rs.3.rs-3240935/v1

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Descriptive Epidemiology of the first outbreak of Lumpy Skin Disease in cattle in Indonesia

https://doi.org/10.21203/rs.3.rs-3240935/v1

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published 07 Aug, 2024

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This study describes the first outbreak of Lumpy Skin Disease (LSD) in cattle in the Bengkalis region, Indonesia and vaccination to control the epidemic. Data on the outbreak and vaccination was obtained from the local veterinary authority of the Bengkalis region, Indonesia. Climatological data was provided by the Meteorological, Climatological, and Geophysical Agency of Riau Province.

Over the 5.5 months period, the outbreak caused 10.4% (94/906) morbidity and 0.6% (6/906) mortality of cattle on infected farms. Temporally, three epidemic waves occurred during the outbreak period. Villages with cattle populations of >150 animals (n=36) were 5.3 times more likely to be infected with LSD compared to villages with smaller cattle populations (n=107) (CI: 2.56 – 10.90, P<0.01). The vaccination campaign covered 43.8% of cattle in villages within a 10 km radius of cases. However, vaccination in villages with larger cattle populations (n=29) was 0.63 less likely to cover 50% of the cattle populations compared to villages with smaller cattle populations (n=41) (CI: 0.39 – 1.02, P=0.05). By the time the first two and the major waves ceased, vaccination had covered only 0.0% (n=6036), 27.8% (n=6,036) and 8.4% (n=6,556) of the cattle in the 10 km radius of the respective waves. The outbreak was statistically associated with rainfall and its interaction with temperature (F(2, 13)=5.822, R²=0.47, P=0.016). This study indicates that the LSD outbreak had low morbidity and mortality. Despite the low vaccination rate, the outbreak ceased, possibly due to plummeting of the abundance of insect vectors.

Lumpy Skin Disease

vaccination

rainfall

cattle

epidemiology

Indonesia

Lumpy Skin Disease (LSD) is an emerging transboundary disease of cattle caused by a Capripox virus and is known to devastate cattle industries worldwide. The economic loss from LSD on cattle farms may be due to a reduced price of the affected animals, mortality, abortion, treatment costs, extra feed additives to boost recovery, labour costs, infertility and reduced milk yield (Chouhan et al., 2022; Kumar et al., 2021; Magori-Cohen et al., 2012). The average loss per case may exceed 100 USD (Chouhan et al., 2022; Molla et al., 2017).

The impact of LSD, however, can vary widely among different localities. Wide ranges of morbidity have been reported in India and Bangladesh, from as low as 0.05–38.34% (Badhy et al., 2021; Sudhakar et al., 2020). Mortality is usually low in an outbreak of LSD in cattle, at less than 3% (Abutarbush et al., 2015; Mat et al., 2021; Uddin et al., 2022). This low mortality may contribute to ignorance amongst farmers of the risk of LSD transmission thus, impair the implementation of control measures in affected regions.

Vaccination is the main control method widely used in populations at risk. Early reporting of a case, culling of diseased animals, and movement restrictions for cattle have been proposed as complementary control measures of LSD, but their implementation in most of the affected regions has been largely unsuccessful due to financial, social and religious constraints (Tuppurainen et al., 2021).

LSD is the latest cattle disease in Indonesia to emerge at the present time. It first affected the Bali cattle population in the Bengkalis region, Riau province and outbreaks have been reported to be spreading southwards and to many parts of Java Island (Salam, 2023). The latest report of LSD in Southeast Asia before Indonesia was from Malaysia in 2021 (Khoo et al., 2022), leading to speculation that the disease was transmitted from this neighbouring country.

A scientific report on the LSD outbreak in Bengkalis is lacking and the impact of the outbreak on the local cattle farming community is unknown. The central government of Indonesia has been providing a subsidized vaccination program to the affected regions but, how the vaccination program progressed in the region is unknown. The success of the ongoing vaccination programs might be impaired due to vaccine quality, the limited number of trained personnel to deliver vaccines, the inaccessibility of animals to be vaccinated and the inadequacy of the cold chain to maintain the vaccine quality. Hence, there is a question of whether the vaccination program was successful or whether alternative strategies to complement the vaccination program are needed. Therefore, the purpose of this present study was to describe the 2022 outbreak of LSD in cattle and evaluate the vaccination program in the Bengkalis region, Riau province of Sumatra Island, Indonesia.

Outbreak investigation and sampling

Twenty-one cattle from 19 farms of five districts suspected of LSD were investigated. These were cases from the districts of Bantan (one case), Bengkalis (three cases), Bukit Batu (10 cases), Siak Kecil (four cases) and Rupat (three cases). An LSD was suspected when multiple lumps with the diameter of about 2–5 cm appeared on the skin of a cattle beast, either localized or generalized (Fig. 1). Samples of blood, skin swab and scrapping of skin lumps were collected, held frozen and sent to the Center of Veterinary Bukittinggi for laboratory tests, using Real Time PCR and ELISA.

Real-Time PCR to detect LSD

Viral DNA was extracted from blood, swab, or tissue scraps using QIAamp Viral DNA Mini Kit, Cat 51306 (Qiagen, Hilden, Germany). The primers and probe used were Forward CaPV-074F1 (5’-AAA ACG GTA TAT GGA ATA GAG TTG GAA-3’), Reverse CaPV-074R1 (5’-AAA TGA AAC CAA TGG ATG GGA TA-3’) and Probe CaPV-074P1 (5’-6FAM-TGG CTC ATA GAT TTC CT-MGBNFQ-3’) (Bowden et al., 2008). The PCR mix was setup at a volume of 20 µL, consisting of Nuclease-free Water 3.2 µL, 2x SesiFAST Probe Lo-ROX Mix, Cat BIO-84005, 10 µL (Meridian, Heidelberg, Germany), Forward Primer (20 µM) 0.6 µL, Reverse Primer (20 µM) 0.6 µL, Probe (10 µM) 0.6 µL, and DNA template 5 µL. The mix was run in a QuantStudio™ 5 Real-Time PCR System (Life Technologies Holdings Pte Ltd, Marsiling Industrial Estate Road 3, Singapore) consisting of a thermal reaction of 10 minutes at 95ºC, followed by 45 thermal reaction cycles of 15 seconds at 95ºC and 60 seconds at 60ºC. A cycle threshold of < 40 was used to deem positive results.

The ELISA of the LSD

All samples were tested using the ID Screen® Capripox Double Antigen Multi-species (IDVet, France) following the manufacturer’s instruction. The wavelength absorbance was read at 450 nm using BioTek ELx800 Absorbance Microplate Reader (BioTek® Instruments, Inc. Highland Park, Winooski, Vermont, USA). Data was presented as an S/P ratio with a cut-off value of ≥ 30% signifying a positive result. All laboratory tests were conducted in the Center of Veterinary Bukittinggi (Balai Veteriner Bukittinggi).

Data of clinical cases and vaccination

Data used in the study included clinical cases and vaccination against LSD from 16 February until 21 Sept 2022, as recorded by the local veterinary authority of the Bengkalis region, Indonesia. After laboratory confirmation of LSD by the Center of Veterinary Bukittinggi, subsequent cases were diagnosed in the field, based on the presence of multiple lumps on the skin with the diameter of about 2–5 cm, which occurred either localized or generalized (Fig. 1).

Data on cattle and farm populations and distributions was collected from records provided by the veterinary authority of Bengkalis region. A few animals were moribund and subsequently slaughtered by the owners; these were included in the calculation of mortality and case fatality rates. Records of rainfall, humidity, temperature, wind speed and wind direction during the outbreak period were provided by the Meteorological, Climatological, and Geophysical Agency of Riau Province.

Data analyses

Data on the outbreak and vaccination was presented descriptively in percentage. The spatial clustering was created in a radius of 10 km from the reported cases, designated as vaccination zone by The Ministry of Agriculture Republic of Indonesia (Kementerian Pertanian RI, 2022).

The epidemic curve was created by grouping cases in ten days interval, based on the following rationale: the blood feeding frequency of a mosquito is estimated to be 0.7 meals per day or approximately once every 34 hours, a second blood feeding is important to allow the breach of the midgut as the abdomen distended from the blood content, and to facilitate the virus to escape into the open circulatory system and invade the salivary gland of the insect (Brackney et al., 2021). Thus, the third blood feedings would be required for an effective transmission of an arbovirus by a mosquito to a naïve host, and that makes the time span from the first to the third blood feeding to be approximately three days (Brackney et al., 2021). Further, the incubation period of LSD ranges from 3–14 days with an average of 7 days (Magori-Cohen et al., 2012). Taken together, an average of 10-day interval would be needed for every new outbreak to emerge.

Climatological data including the average of ten-day rainfalls, humidity and temperature were plotted with cases group in the subsequent ten days interval in a multiple linear regression statistic to analyze the association between climatologic parameters and the emergence of cases, the coefficient of determination (R²) was presented with P-value. Ratios of the outbreak and the vaccination rate were compared between villages with large cattle population and small population, along with P-value and 95% confidence interval.

Maximum Wind speed and its direction was matched with the primary case of the epidemic in the eight districts, to develop putative transmission pathways of the outbreak amongst infected districts, assuming the winds blew insect vectors. The downwind dispersion day was deemed when the wind speed exceed 5 km/h (Service, 1997) during the incubation period; the 3th − 14th days prior to the primary case on a district (Magori-Cohen et al., 2012). A total of 12 days of wind blows prior to a primary case was thus used in the analysis. A source of infection was considered when at least there was a day in the 12 observed days where the wind speed exceeded 5 km/h blew to a newly infected district from an already infected district. Data was presented visually in figure.

Description of the outbreak

All the 21 cases tested positive by PCR or ELISA. These included cases from the districts of Bantan (one case, PCR), Bengkalis (three cases, PCR), Bukit Batu (10 cases, PCR), Siak Kecil (four cases, PCR) and Rupat (three cases, ELISA).

Table 1 shows that eight out of 11 districts in the region were affected by the LSD outbreak. During the 168 days outbreak period (16 February - 02 August 2022), 94 cases were observed. The duration of an outbreak in a district ranged from 1 – 64 days, with an average of 20.8 days. The districts of Bukit Batu, Siak Kecil and Bathin Solapan suffered the longest outbreaks (64, 52 and 29 days respectively). The distance between two districts with two consecutive outbreaks ranged between 20 – 85 km. The time intervals between two consecutive primary cases in different districts ranged from 9 – 36 days. An exception was the primary case reported in the district of Pinggir, which occurred 80 days after the preceding primary case in the Bathin Solapan.

The outbreak affected 1.2% (n=43) of 3,582 farms in 20.7% (n=25) of 121 villages in the eight districts. The outbreak caused 10.4% (94/906) morbidity and 0.6% (5/906) mortality of cattle on infected farms. The case fatality rate was 5.3% (5/94). The incidence rate on the infected farms was 6 cases per 10,000 animal-day. In the 94 cases, lumps were the single most observed clinical sign (37.2%) or occurred along with nasal discharge (33.0%) or with a crust on the lumps (29.8%).

The outbreak was grouped into three spatial clusters: 1) the Bengkalis cluster included the districts of Bantan, Bengkalis, Bukit Batu and Siak Kecil, where the index case was reported on 16 Feb 2022 in the Bantan; 2) the Rupat cluster included only the district of Rupat, with the primary case on 29 April 2022 and; 3) the Mandau cluster, included the districts of Mandau, Bathin Solapan and Pinggir, the primary case was reported on 10 May 2022 in the Mandau. Data plotting on primary cases, wind speed and wind directions indicated that the wind-borne transmissions moved mainly to the southwest directions. The wind-borne incursion of LSD to Bantan and Rupat districts might possibly have originated from the neighboring Malaysian Peninsula. From the Bantan, the epidemic might spread to the Bukit Batu, Bengkalis, and Siak Kecil. Additionally, the Rupat might have been also infected from the Bantan cluster and, from the Rupat, the LSD might spread to the Mandau cluster (Table 1, Figure 2).

The epidemic curve indicates that the outbreak occurred in three waves (Figure 3): the first small wave involved the districts of Bantan, Bukit Batu and Bengkalis. The second wave involved the districts of Bukit Batu and Siak Kecil, while the major wave occurred in the districts of Bukit Batu, Siak Kecil, Rupat, Bathin Solapan and Mandau. The first wave lasted from 16 Feb to 8 March 2022, the second from 8 March to 17 April 2022 and the major wave occurred between 17 April and 16 June 2022. Sporadical cases occurred from 26 July until 2 Aug 2022, in Bathin Solapan and Pinggir districts.

Vaccination against LSD

The Bengkalis region has 155 villages, 143 villages of which have cattle populations. Vaccination planned to target 95 villages in the eight affected districts. It included 25 infected villages and the surrounding 70 non-infected villages in vaccination zones (Kementerian Pertanian RI, 2022). Vaccination commenced on 17 March until 21 September 2022, covered 73.7% (70/95) of the target villages, but only 47.0% (5,517/11,733) of cattle in the target villages. In detail, 92.0% (23/25) of infected villages were vaccinated, covering 49.1% (2,436/4,958) of their cattle population, while 67.1% (47/70) of non-infected villages in the vaccination zones were vaccinated, covering 45.5% (3,081/6,775) of their cattle populations (Table 2).

Vaccination campaigns were divided into two rounds. The first round was conducted in the areas of the first two epidemic waves, covering 49.7% (3,002/6,036) of cattle in target villages, in the districts of Bantan, Bukit Batu, Siak Kecil and Bengkalis, completed within 105 days, from 17 March – 30 June 2022. By the time the first two waves stopped, the vaccination had been covering only 0.0% (0/6036) and 27.8% (1,676/6,036) of the targeted cattle population. The second round of vaccination was to cope with the major epidemic, completed within 118 days from 26 May - 21 September 2022. It covered 44.1% (2,515/5,697) of cattle in four districts in the vaccination zone; Rupat, Bathin Solapan, Mandau and Pinggir. By the day the major wave stopped, vaccination had covered only 9.7% (550/5,697) of the cattle population in the target villages.

The proportion of LSD-infected villages was 5.3 times larger in villages with cattle populations of >150 animals (n=36) than in villages with cattle population of ≤150 animals (n=107) (CI: 2.56 – 10.90, P<0.01). Similarly, in villages that were vaccinated against LSD, the proportion of LSD-infected villages in villages with cattle population of >150 animals (n=29) was 2.2 times larger than that in villages with cattle population of ≤150 animals (n=41) (CI: 1.10 – 4.38, P=0.04). However, the proportion of villages with a vaccination rate of >50% in villages with cattle population of >150 animals (n=29) was 0.63 lower than that in villages with cattle population of ≤150 animals (n=41) (CI: 0.39 – 1.02, P=0.05) (Table 3).

The first two waves ceased two months and a half month before the Eid Al-Fitri festival in 2^nd May 2022 and the major wave ended almost a month before Eid Al-Adha in the 10^th July 2022. Multiple linear regression statistic showed a positive association between the average of ten-day rainfall and temperature, and the ten-day cumulative frequency of cases in the next 10 days, with the formula of Cases=-62.787*rain+95.018*rain*temperature*0.025 (F(2, 13)=5.822 , P=0.016, R²=0.47, variables rain and temperature added to the prediction at P=0.006).

This is a report on the first outbreak of and control efforts against LSD in cattle in Riau, Indonesia. The epidemic lasted for five and a half months and clustered into three areas. The epidemic caused only low morbidity (10.6%) and mortality (0.6%) and ended, although the coverage by vaccination was limited. Many clinical cases however, may not have been reported to the local authorities and the true morbidity may be higher than the number presented here.

Statistically, the epidemic waves were moderately associated with increased precipitation and temperature during the ten preceding days. These and environmental factors such as slope, land cover, and elevation were considered contributing to the onset of LSD outbreak in the Middle East (Alkhamis and VanderWaal, 2016; Ardestani and Mokhtari, 2020). LSD is transmitted by blood sucking vector insects such as Stomoxys flies, mosquitoes, midges or ticks (Sprygin et al., 2019), whose regeneration and abundance may follow precipitation and temperature (Khatchikian et al., 2010). The abundance of Stomoxys flies was considered to be associated with LSD on dairy farms (Gubbins, 2019; Kahana-Sutin et al., 2017) and Aedes mosquito was reported to be the second most important vector for LSD (Gubbins, 2019). It remains unclear which insects play the most important role in the transmission of LSD in the study region. However, this finding indicates that mitigations against LSD may need to consider the pattern of precipitation and temperature in a region.

Wind in this study were mostly observed to be in a South-westerly direction, and might have facilitated LSD transmission from two areas on the Malaysian peninsula. Although the transmission of insect borne diseases through livestock transport has also been speculated upon (Medley et al., 2015), this mode of transmission, if it occurs, might not necessarily immediately spark an outbreak. The current study showed that the waves of the LSD outbreak in the region had ceased long before the period of preparation for the Eid Al-Fitr and Eid Al-Adha. During the authors’ experience working in the study area for years, transport of cattle across districts usually peaks two weeks preceding these festivities and are higher preceding Eid Al-Adha. Infected vectors may be transported along during the periods as, control of livestock disease through highway transport in the region is ineffective due to facility shortages (Nugroho et al., 2022). However, in this study such transmission or a possible direct association with the LSD outbreak was not apparent.

The vaccination strategy in the study area, which covered a 10 km radius from reported cases potentially protects an area twice larger than the home ranges of mosquitoes (Harrington et al., 2005; Kementerian Pertanian RI, 2022; Russell et al., 2005; Service, 1997). However, the vaccination rate was less than half of the total cattle population within the targeted area. Moreover, villages with larger cattle population were likely to have a lower rate of vaccination, while they were at five times larger risk of an outbreak of LSD, compared to villages with smaller cattle populations. Interestingly, the epidemic halted before vaccination rate reached one third of the target population in the first two waves and the major wave stopped when the second round of vaccination just commenced thus, the value of vaccination in bringing this epidemic to an end, remains in question.

In conclusion, the first LSD outbreak in the Bengkalis region caused low morbidity and mortality. Villages with larger cattle populations were at higher risk of being infected with LSD but, their vaccination rate was lower than that of villages with smaller cattle population. Observations on the precipitation and temperature might help with predicting the onset of an LSD outbreak in a district and designing methods to control the LSD.

Acknowledgement

Authors would like to thank Gigih Tri Pambudi, DVM., MM, the director of laboratory of Veterinary Bukittinggi for supports during laboratory works. Authors appreciate the regional government of Bengkalis for permission with the study. Authors appreciate cattle farmers in the region of Bengkalis for their cooperation during the outbreak investigation and vaccination.

Author contributions

Widi Nugroho: Conceptualization; Formal analysis; Funding acquisition; Methodology; Project administration; Resources; Supervision; Validation; Visualization; Roles/Writing - original draft; Writing - review & editing; Hani Muhammad Mardani: Conceptualization; Data curation; Formal analysis; Funding acquisition; Investigation; Methodology; Project administration; Resources; Supervision; Validation; Visualization; Writing - review & editing; Michael Philipp Reichel: Conceptualization; Formal analysis; Funding acquisition; Methodology; Supervision; Validation; Visualization; Writing - review & editing; Yul Fitria: Performed research;; Resources; Formal analysis; Roles/Writing - original draft; Writing - review & editing; Yuli Miswati: Performed research; Resources; Formal analysis; Roles/Writing - original draft; Writing - review & editing; Niko Febrianto: Data curation; Investigation; Resources; Formal analysis; Roles/Writing - original draft; Writing - review & editing; Muhammad Edy Nuryanto: Performed research; Resources; Supervision; Writing - review & editing; Intan Apriana: Performed research; Resources; Supervision; Writing - review & editing; Nur Azzahrawani: Project administration; Resources; Supervision; Validation; Writing - review & editing; Shelly Kusumarini:Formal analysis; Roles/Writing - original draft; Writing - review & editing; Hermanto: Performed research;; Aji Pamungkas Riau Sahrul Ramadan: Performed research;; Deci Nanda Nurdiana: Performed research; Agus Praminto: Performed research. All authors read and approved the final manuscript.

Funding

This study was funded by ACIAR (Australian centre for International Agricultural Research) through the project ARSF3, project code: 043-Widi Nugroho-Indonesia, organized by The University of New England, Australia.

Data

Availability of data and material Data can be accessed upon request to the corresponding author.

Ethics approval The study was approved by the regional government of Bengkalis, Riau, Indonesia, with document number 061/DPMPTSP-JU/X/2022/705.

Consent to participate Not applicable.

Consent for publication Not applicable.

Competing interests The authors declare no competing interest.

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Table 1. Chronology of the Lumpy Skin Disease outbreak in cattle in the Bengkalis region, Indonesia, 2022

District	Duration of the outbreak	Duration (days)	Interval* (days)	Distance^ǂ (~km)	Infected villages (villages with cattle population)	Infected farms (farms in the district)	Clinical cases (cattle on infected farms)	Mortality on infected farms (%)
Bantan	16-Feb	1	9	40	1 (21)	1 (272)	3 (33)	0
Bukit Batu	25 Feb - 29 Apr	64	9	25	5 (10)	15 (334)	20 (91)	3 (3.2)
Bengkalis	06-Mar	1	18	35	3 (27)	3 (297)	3 (12)	0
Siak Kecil	24 Mar - 14 May	52	36	85	4 (17)	10 (1,026)	15 (93)	2 (2.2)
Rupat	29 Apr - 07 May	9	11	60	3 (15)	3 (634)	5 (60)	0
Mandau	10 - 18 May	9	13	20	3 (7)	4 (396)	6 (50)	0
Bathin Solapan	13 May - 07 Jun	29	80	20	5 (11)	6 (288)	41 (561)	0
Pinggir	02-Aug	1	-	-	1 (13)	1 (335)	1 (6)	0
Total	16 Feb - 02 Aug	-	-	-	25 (121)	43 (3,582)	94 (906)	5 (0.6)

* Interval between the primary case in a district and the primary case in the next infected district

^ǂ Distance between the location of the primary case in a district to the location of the subsequent primary case in a different district

Table 2. Vaccination against Lumpy Skin Disease of cattle in districts of the Bengkalis region, Indonesia, 2022

District	Villages in the Vaccination zone*	Total villages vaccinated	Length of the Outbreak	Period of the vaccination	Interval between primary case and vaccination (days)	Cattle vaccinated	Cattle Population in the vaccination zone
Bantan	14	12	16-Feb	22 Mar - 25 May	34	342	631
Bukit Batu	10	8	25 Feb - 29 Apr	17 Mar - 25 Jun	20	381	1,058
Bengkalis	21	14	06 Mar - 21 Mar	23 Mar - 29 Jun	17	585	796
Siak Kecil	17	16	24 Mar - 14 May	17 Mar - 30 Jun	-7	1,694	3,551
Rupat	8	5	29 Apr - 07 May	26 May - 21 Sept	27	1,475	2,072
Mandau	7	5	10 May - 18 May	07 Jun - 31 Aug	28	268	1,305
Bathin Solapan	11	6	13 May - 07 Jun	01 Jun - 25 Aug	19	575	1,329
Pinggir	7	4	02 Aug	09 Jun - 01 Jul	-54	197	991
Total	95	70	16 Feb - 2 Aug	17 Mar - 21 Sept	-	5,517	11,733

* Vaccination zone is an area at a radius of 10 km from the cases reported (Kementerian Pertanian RI, 2022)

Table 3. Cattle population, infected and vaccinated villages in the Bengkalis region, Indonesia, 2022

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published 07 Aug, 2024

Read the published version in Tropical Animal Health and Production →

Editorial decision: Major revision with re-assessment
24 Mar, 2024
Reviewers agreed at journal
23 Jan, 2024
Reviewers invited by journal
29 Oct, 2023
Editor assigned by journal
15 Aug, 2023
First submitted to journal
11 Aug, 2023

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Descriptive Epidemiology of the first outbreak of Lumpy Skin Disease in cattle in Indonesia

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Journal Publication

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Abstract

Figures

Introduction

Materials and methods

Outbreak investigation and sampling

Real-Time PCR to detect LSD

The ELISA of the LSD

Data of clinical cases and vaccination

Data analyses

Results

Description of the outbreak

Vaccination against LSD

Discussion

Declarations

References

Tables

Status:

Journal Publication

Version 1